The Marin Headlands was originally home to the Native American Coastal Miwok, who lived seasonally here for thousands of years. In the 18th century, Spanish and Mexican ranchers occupied the land, eventually giving way to Portuguese immigrant dairy farmers. In the 1890s, the first military installations were built to prevent hostile ships from entering San Francisco Bay. The Fort Barry buildings were erected from 1907 to 1913 and served as an active military center until 1950.

The National Park Service took over the decommissioned buildings in 1972, inviting several mission-based nonprofits to act as park partners and specifically writing an arts center into the park’s Master Plan. In 1982, a founding Board of Directors of local artists, activists, and civic leaders incorporated Headlands Arts Center (renamed Headlands Center for the Arts in 1989). The organization launched an ambitious plan to rehabilitate the historic buildings through artists’ commissions, empowering artists to re-envision the physical space and future use of the facility. In 1994, the organization secured a twenty-year agreement with Park Service for use of the Fort Barry buildings.